Upper extremity motor abilities and cognitive capability mediate the causal dependency between somatosensory capability and daily function in stroke individuals

Stroke individuals’ daily function has been demonstrated to be influenced by their somatosensory capability, cognitive capability, and upper extremity (UE) motor abilities. However, the structural relationships among these abilities on stroke individuals’ independence in daily function remain unclear. We analyzed the pretest measures of 153 stroke individuals in outpatient rehabilitation settings by structural equation modeling to determine the structural relationship among somatosensory capability, UE muscle strength, UE motor function, and cognitive capability that influences independence in daily function. The standardized results indicated somatosensory capability negatively influenced UE muscle strength, but positively influenced UE muscle strength mediated by UE motor function. UE muscle strength, then, positively influenced individuals’ independence in daily function. On the other hand, somatosensory capability positively influenced cognitive capability, which marginally and positively affected the performance of independence in daily function. To the best of our knowledge, this is the first study to demonstrate the influence of somatosensory capability on the daily function is mediated mainly by motor functions and marginally by cognitive capability. This structural model may allow future clinical therapists to design more effective task-related training protocols to promote the independence in daily function for stroke individuals.


Outcome measures.
Measures of somatosensory capability. The Revised Nottingham Sensory Assessment (rNSA) was used to evaluate the sensation of stroke individuals, and its psychometric properties have been established 25 . It consists of 72 items grouped into three subscales measuring tactile sensation, proprioception, and stereognosis. The Tactile Sensation subscale includes light touch, temperature, pinprick, pressure, tactile localization, and bilateral simultaneous touch and is administered to the face, trunk, shoulder, elbow, wrist, hand, knee, ankle, and foot. The rNSA is scored on a 3-point ordinal scale (0-2), with a lower score suggesting greater somatosensory impairment.
Measures of UE muscle strength. The Medical Research Council scale (MRC) is an ordinal scale that assesses the UE muscle strength in stroke individuals, and the reliability of this measurement is good to excellent 26 . This scale measures wrist extension, finger extension, elbow flexion and shoulder abduction on both sides. The scoring for each muscle ranges from 0 to 5, with a higher score indicating stronger muscle.

Measures of UE motor function. The Wolf Motor Function Test (WMFT) and the Chedoke Arm and Hand
Activity Inventory (CAHAI) were used to assess the functional ability of the stroke individual's UE. The WMFT was developed by Wolf and colleagues to quantitatively assess UE motor function 27 . The WMFT-time measures the time required to complete the tasks, and the WMFT-quality assesses functional ability on a 6-point ordinal scale. A lower WMFT-time performance indicates faster movement, and a higher WMFT-quality score suggests better quality of movement. The reliability of the WMFT is excellent 28 . The CAHAI is used to evaluate the functional ability of the paretic UE to perform tasks. It uses a 7-point quantitative scale to measure the client's ability to complete the task using their bilateral hand. A higher score indicates that patients have better ability to complete the functional movement independently. The reliability and the internal consistency of the CAHAI is good in individuals with stroke 29 .
Measures of general cognitive capability. The Montreal Cognitive Assessment (MoCA) was used as a general measurement of cognitive capability in this study. This assessment tool is a 30-point test 30 . The MoCA has been recommended as a valid and reliable clinical assessment in stroke individuals 31 .
Measures of the independence in daily function. The Nottingham Extended Activities of Daily Living Scale (NEADL) is a self-report scale that measures IADL. It evaluates 4 areas of daily function, including mobility, kitchen, domestic, and leisure activities. The total score is 66, and a higher score indicates better daily functional ability. The psychometric properties of the NEADL have been well established 32 .
Statistical analysis. The statistical analyses for this study were generated using SAS/STAT 9.4 software with the CALIS procedure (SAS Institute Inc, Cary, NC). A P value of ≤ 0.05 was considered to indicate statistical significance. The participants' demographic characteristics are summarized with descriptive statistics.
To examine the structural relationships among these measures, we used the covariance-based SEM technique, which is a multivariate statistical analysis technique for representing, estimating, and testing a theoretical network of linear relationships among a set of measured variables and latent constructs 21 . In this study, the construct of somatosensory capability was measured by the 3-item parcels of the rNSA (tactile sensation, proprioception, and stereognosis). The construct of the UE muscle strength was measured by the 4-item parcels of the MRC. The construct of UE motor function was evaluated by the assessments of the WMFT time, the WMFT quality, and the CAHAI score. The 7-item parcels of the MoCA indicated the construct of cognitive capability. Finally, the 4-item parcels of the NEADL were used to indicate the construct of independence in daily function. In this study, although several ordinal measured variables (such as rNSA, CAHAI, and NEADL) were used, these ordered categorical data have at least five categories so that they could be treated as continuous variables in using SEM 33,34 .
The confirmatory factor analysis (CFA) was used to evaluate the goodness of fit of the measurement model containing the 5 latent constructs (factors) and 21 measured variables. To examine the fit of the structural model, the directional relationship of the latent constructs to the model of independence in daily function was determined by SEM. Maximum likelihood estimation was used to estimate factor loading, path coefficient, and the amount of measurement error.
No single model-fitting index can consider all scenarios 35 , so we used indicators with different characteristics to evaluate the goodness of fit of the hypothesized model. According to recommendations of previous research 36,37 , the fit of the measurement and structural model was assessed with the P value of the χ 2 statistic > 0.05 (P > 0.05), χ 2 /degree of freedom (df) of < 2, comparative fit index (CFI) of > 0.95, root mean square error of approximation (RMSEA) of < 0.05, and standardized root mean residual (SRMR) of < 0.08.
Considering the theoretical and empirical significance of the associations among these latent constructs, the entire model was revised by the suggestion of the multivariate Lagrange Multiplier (LM) and Wald test to improve the goodness of fit of the model 38 . The multivariate LM test identifies parameters that would lead to the largest drop in the model χ 2 and calculates the expected change in χ 2 , thus we can add these parameters to the model (i.e., added a covariance between error terms of variables) to improve the model fitting. The Wald test is analogous to backward deletion of variables in stepwise regression, where one seeks a nonsignificant change in R 2 when variables are left out.

Results
This study collected the evaluation data of 153 stroke individuals (109 men), with a mean age of 56.19 ± 11.71 years. Table 1 summarizes the demographic and clinical characteristics as well as evaluation data of the participants. Table 2 shows the association between observed variables.
CFA of the measurement model. The goodness of fit of the measurement model showed that the model had good fit with an RMSEA of 0.049 (< 0.05), and SRMR of 0.077 (< 0.08), but the CFI did not achieve the criteria of fit (CFI, 0.948). Although the χ 2 value was significant (χ 2 = 243.851, df = 179, P = 0.001), the χ 2 /df was < 2 (χ 2 /df = 1.362), which provided a reasonable model fit.
Because the indicators did not provide consistent fitting results, we revised the measurement model based on the recommendations of the LM test to improve the goodness of fit on all indicators. We added a path from the cognitive capability to the item of leisure activity in NEADL as well as the covariance between shoulder and elbow muscle strength, and the modification index values of these 2 parameters were 23.378 and 22.323, respectively. The goodness of fit of the revised model showed a good fit (χ 2 = 194.796, df = 177, P = 0.171; χ 2 /df = 1.101; CFI = 0.986; RMSEA = 0.026; SRMR = 0.062). Figure 1 shows the CFA results of the revised measurement model. Figure   To improve the precision of our hypothesized model, we used the Wald test to determine path(s) that could be reasonably removed without compromising the goodness of fit of the model. The results of the Wald test showed that 2 paths did not significantly influence the variance of the χ 2 value (P > 0.06 for both). Considering that the path from cognitive capability to the independence in daily function showed a marginal but not significant effect (χ 2 = 3.310, df = 2, P = 0.069) and that previous studies have demonstrated the important role of the cognitive capability in the daily function 19,20 , we only removed the path from UE motor function to the independence in daily function (χ 2 = 0.002, df = 1, P = 0.961) in the model. Figure 2b shows the path diagram of the revised model. All model-fitting indices showed good fit (χ 2 = 195.954, df = 181, P = 0.212; χ 2 /df = 1.083; CFI = 0.988; RMSEA = 0.023; SRMR = 0.064). In the standardized results, the somatosensory capability positively influenced the UE motor function performance (β = 0.368, P < 0.001) and the cognitive capability (β = 0.292, P = 0.001) but negatively influenced the UE muscle strength (β = − 0.202, P = 0.004). The UE motor function significantly influenced the UE muscle strength (β = 0.909, P < 0.001), and the UE muscle strength significantly influenced the independence in daily function (β = 0.208, P = 0.020).

Discussion
To the best of our knowledge, this is the first study using SEM to demonstrate the influence of the relationship among somatosensory capability, UE muscle strength, UE motor function, and cognitive capability on the independence in daily function in chronic stroke individuals. The results (see Fig. 2b) indicate that independence in daily functions of stroke individuals would be affected by their somatosensory capability via 2 different pathways. One is mediated by their motor-related capabilities (i.e., somatosensory-motor pathway) (see the left part of Fig. 2b), and the other is mediated by their cognitive capability (i.e., somatosensory-cognitive pathway) (see the right part of Fig. 2b). Mediation effect refers to the transmission of the effect of an independent variable (i.e., somatosensory capability) on a dependent variable (i.e., independence in daily function) through other variables (i.e., UE motor function, UE muscle strength, cognitive capability) 39 .
In the somatosensory-motor pathway (see the left part of Fig. 2b), improving patients' somatosensory capability could enhance their independence in daily function either by enhancing their UE motor function performance, which in turn increased the UE muscle strength, or by directly reducing their UE muscle strength. This finding was consistent with results of previous studies that the restoration of the somatosensory capability has positive impact on the improvement of UE motor function and the independence in daily function in stroke individuals 10,11 , and UE muscle strength of the affected hand was associated with independence in daily function 6 . More importantly, the results further clarify the role of UE muscle strength in the relationship among somatosensory capability, UE motor abilities and independence in daily function, which was not mentioned in the previous research.
Regarding the role of UE muscle strength in the somatosensory-motor pathway (see the left part of Fig. 2b), intact or good somatosensory capacities might provide appropriate and sufficient somatosensory input to the brain for assisting in planning a motor output or learning a correct motor program for execution 40,41 . Accordingly, somatosensory information enhances the learning or the performance of functional use of the affected arm. Once the affected arm function improved, the stroke individuals might use the affected arm to practice a variety of tasks in a greater amount and increase the UE muscle strength. On the other hand, the pain sensations www.nature.com/scientificreports/ associated with the muscle spasticity and contractures 42 may also increase with the enhancement of somatosensory capacities, thereby reducing the UE muscle strength 43 . One of the most common pain syndromes after stroke is the muscle spasticity and contractures with hemiplegia 44 . These hypertonic contractions usually present with stiffness during flexion of the upper limbs, and the prevalence of spasticity-related pain tends to peak at the chronic stage 45 . Spasticity and contractures can also cause spontaneous, painful spasms and night cramps, which can damage muscles and joints. In this case, the UE muscle strength should be reduced, because the pain sensations induced by the muscle spasticity and contractures can cause a certain degree of stiffness and tiredness in the muscles of the affected UE. These 2 routes of the somatosensory-motor pathway (see the left part of Fig. 2b) significantly influenced the independence in daily function. However, the overall influence of somatosensory capability on UE muscle strength would be positive because the effect of the route of sensation-affected UE motor function-UE muscle strength was greater than the effect of the route of sensation-UE muscle strength.
In summary, when the ability of stroke individual's UE motor function plays a mediation role, somatosensory capability would show positive influence on UE muscle strength; however, somatosensory capability has negative influence on the UE muscle strength. An individual's independence in daily function is only influenced by their UE muscle strength, and UE motor function only shows the impact when it is mediated by the UE muscle strength, indicating appropriate UE muscle strength is a critical factor improving the performance of independence in daily function. Only focusing on the improvement of a patient's functional UE performance may not guarantee the restoration of their independence in daily function.
This study identified the causal relationship between UE motor abilities and independence in daily functions, thus confirming and extending the previous findings, which only demonstrated the association between UE motor ability and the performance of independence in daily function 7 . More importantly, the current model shows that increasing the function performance of the UE should be accompanied by an improvement in its UE muscle strength. UE muscle strength thus has a key role in determining the outcome of an individual's somatosensory-motor rehabilitation.
In the somatosensory-cognitive pathway (see right part of Fig. 2b), the enhancement of stroke individuals' somatosensory ability can improve their cognitive capability, which in turn influenced their independence in daily function. Previous studies showed an association between cognitive capabilities and the performance of daily functions in stroke individuals has been demonstrated 19,20 . This study extended the previous study finding to underscore the impact of the cognitive enhancement on the independence in daily function of stroke individuals. Our finding showed that cognitive capability has a marginal contribution to the variance in the measures of the IADL performance (P = 0.053). It is consistent with the early findings that motor deficits had a larger impact than did perceptual and cognitive deficits on the daily function 46,47 and may partially support the evidence that cognitive impairment does not influence functional status recovery in stroke individuals 48 .
The marginally impact of cognitive capability on the performance of independence in daily function in this study may be due to the cognitive level of the stroke individuals included and the diverse effects of different cognitive components (attention, memory, executive function, etc.) on the measurements of IADL. Given that stroke individuals preserve good general cognitive capacities, as measured by MoCA, and that independence in daily function involves familiar and routine usual activities, the patients might be capable of performing these daily tasks automatically without great involvement of cognitive processes, leading to a small impact of cognitive capabilities on the IADL performance.
On the other hand, Stephens et al. 49 identified the differential relationships between different components of cognitive impairment (attention, executive performance, and memory) and the impairments of daily function for stroke individuals without dementia. They found that the memory deficit was not associated with any of these daily function components but that the impairments of attention and executive function were associated with disabilities in self-care tasks and the impairment of general cognition with the impairment of complex self-management tasks. Future research is needed to examine the impact of different cognitive domains on performance of independence in daily functions. It may provide inspiration for the development of clinical treatment methods in which differences in cognitive components are considered to design the most appropriate rehabilitation program to reestablish the independence in daily function.
The model provided by the current study shows the contribution of the somatosensory capability, cognitive capability, and UE motor abilities to the degree of the independence in daily function of stroke individuals. This model not only enhances our understanding of the mechanisms between these factors and the stroke individual's ability to perform the independence in daily function but also might shed light on the possible directions for providing personalized treatment protocols for stroke individuals.
This study has a number of limitations. First, further studies with larger sample sizes 50,51 and more indicators per factor 50,52 are needed to determine the reliability and validity of this model structure.
Second, we only found a marginal effect of cognitive ability on performance of independence in daily function. As suggested by the previous findings, only specific cognitive components (i.e., attention and memory) may be critical. Future studies should be conducted to confirm the role of different cognitive components in the recovery of the independence in daily function of stroke individuals.
Finally, this study only collected the cross-sectional data on stroke individuals without severe cognitive impairment (MMSE > 20) and were younger than typical stroke populations (74.3 ± 13.6), and male participants accounted for a higher proportion of our sample 53 . The structural model may not be applicable to the entire stroke population (e.g., subacute and acute stroke, moderate to severe cognitive impairment). To increase the generalizability of the model, future studies should use data from stroke individuals with diverse characteristics. www.nature.com/scientificreports/ Publisher's note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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